The aphid transmission factor of cauliflower mosaic virus forms a stable complex with microtubules in both insect and plant cells

Blanc, Stéphane; Schmidt, Isabelle; Vantard, M.; Scholthof, Karen‐Beth G.; Kuhl, G.; Espérandieu, Pascal; Cérutti, Martine; Louis, C.

doi:10.1073/pnas.93.26.15158

Cited by 41 publications

(24 citation statements)

References 32 publications

(33 reference statements)

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“…Fig. 2 A and B shows that, in coinfected Sf9 cells, P2 and P3 indeed colocalize in de novo inclusion bodies whereas infection solely with a P2-encoding baculovirus resulted in formation of typical paracrystals as reported (8,23). In contrast, infection with a P3-encoding baculovirus alone gave rise to uniform distribution of P3 throughout the cell (Fig.…”

Section: Resultsmentioning

confidence: 83%

Intracellular distribution of viral gene products regulates a complex mechanism of cauliflower mosaic virus acquisition by its aphid vector

Drucker

Froissart

Hébrard

et al. 2002

Proc. Natl. Acad. Sci. U.S.A.

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Interactions between Cauliflower mosaic virus (CaMV) and its aphid vector are regulated by the viral protein P2, which binds to the aphid stylets, and protein P3, which bridges P2 and virions. By using baculovirus expression of P2 and P3, electron microscopy, surface plasmon resonance, affinity chromatography, and transmission assays, we demonstrate that P3 must be previously bound to virions in order that attachment to P2 will allow aphid transmission of CaMV. We also show that a P2:P3 complex exists in the absence of virions but is nonfunctional in transmission. Hence, unlike P2, P3 and virions cannot be sequentially acquired by the vector. Immunogold labeling revealed the predominance of spatially separated P2:P3 and P3:virion complexes in infected plant cells. This specific distribution indicates that the transmissible complex, P2:P3:virion, does not form primarily in infected plants but in aphids. A model, describing the regulating role of P3 in the formation of the transmissible CaMV complex in planta and during acquisition by aphids, is presented, and its consequences are discussed.

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Section: Resultsmentioning

confidence: 83%

Intracellular distribution of viral gene products regulates a complex mechanism of cauliflower mosaic virus acquisition by its aphid vector

Drucker

Froissart

Hébrard

et al. 2002

Proc. Natl. Acad. Sci. U.S.A.

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“…7) indicates a strong binding between P6 and microtubules. Although we do not yet know whether this is a direct interaction, a similarly strong binding was demonstrated for CaMV P2 and TMV MP, which were both also shown to stabilize microtubules (Blanc et al, 1996;Ashby et al, 2006). One possible explanation for the association is that microtubules may serve as a framework for inclusion body assembly.…”

Section: P6 Associates With and Stabilizes Microtubulesmentioning

confidence: 74%

“…Interestingly, the CaMV gene II product (P2), an aphid transmission factor, was previously shown by immunoelectron microscopy to associate with microtubules in both insect and plant cells, although the significance of this interaction remains unclear (Blanc et al, 1996). In addition to these two viral proteins found to colocalize with microtubules in planta, the Hsp70 homolog from Beet yellows virus and the coat protein from PVX have both been shown to interact with microtubules in vitro (Karasev et al, 1992;Serazev et al, 2003).…”

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confidence: 99%

The Cauliflower Mosaic Virus Protein P6 Forms Motile Inclusions That Traffic along Actin Microfilaments and Stabilize Microtubules

et al. 2008

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The gene VI product (P6) of Cauliflower mosaic virus (CaMV) is a multifunctional protein known to be a major component of cytoplasmic inclusion bodies formed during CaMV infection. Although these inclusions are known to contain virions and are thought to be sites of translation from the CaMV 35S polycistronic RNA intermediate, the precise role of these bodies in the CaMV infection cycle remains unclear. Here, we examine the functionality and intracellular location of a fusion between P6 and GFP (P6-GFP). We initially show that the ability of P6-GFP to transactivate translation is comparable to unmodified P6. Consequently, our work has direct application for the large body of literature in which P6 has been expressed ectopically and its functions characterized. We subsequently found that P6-GFP forms highly motile cytoplasmic inclusion bodies and revealed through fluorescence colocalization studies that these P6-GFP bodies associate with the actin/endoplasmic reticulum network as well as microtubules. We demonstrate that while P6-GFP inclusions traffic along microfilaments, those associated with microtubules appear stationary. Additionally, inhibitor studies reveal that the intracellular movement of P6-GFP inclusions is sensitive to the actin inhibitor, latrunculin B, which also inhibits the formation of local lesions by CaMV in Nicotiana edwardsonii leaves. The motility of P6 along microfilaments represents an entirely new property for this protein, and these results imply a role for P6 in intracellular and cell-to-cell movement of CaMV.

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“…CaMV forms intracellular replication compartments as well as a specialized transmission body in its plant host. CaMV aphid transmission factor (ATF) forms paracrystalline structures that bind and stabilize MTs (139). Remarkably, transmission bodies react within seconds to the presence of aphids on the plant by rapid disruption and redistribution of the core transmission body helper protein, P2, onto MTs, driving the release of virions from the transmission body and factories onto MTs.…”

Section: Mt Functions During Infection Of Plants Insects and Bacteriamentioning

confidence: 99%

Microtubule Regulation and Function during Virus Infection

Naghavi

Walsh

2017

J Virol

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Microtubules (MTs) form a rapidly adaptable network of filaments that radiate throughout the cell. These dynamic arrays facilitate a wide range of cellular processes, including the capture, transport, and spatial organization of cargos and organelles, as well as changes in cell shape, polarity, and motility. Nucleating from MT-organizing centers, including but by no means limited to the centrosome, MTs undergo rapid transitions through phases of growth, pause, and catastrophe, continuously exploring and adapting to the intracellular environment. Subsets of MTs can become stabilized in response to environmental cues, acquiring distinguishing posttranslational modifications and performing discrete functions as specialized tracks for cargo trafficking. The dynamic behavior and organization of the MT array is regulated by MT-associated proteins (MAPs), which include a subset of highly specialized plus-end-tracking proteins (ϩTIPs) that respond to signaling cues to alter MT behavior. As pathogenic cargos, viruses require MTs to transport to and from their intracellular sites of replication. While interactions with and functions for MT motor proteins are well characterized and extensively reviewed for many viruses, this review focuses on MT filaments themselves. Changes in the spatial organization and dynamics of the MT array, mediated by virus-or host-induced changes to MT regulatory proteins, not only play a central role in the intracellular transport of virus particles but also regulate a wider range of processes critical to the outcome of infection.KEYWORDS virus, cytoskeleton, microtubules, nucleation, microtubule-associated proteins, plus-end-tracking proteins T he dense cytosolic environment poses a major barrier to the free movement of macromolecules, making microtubule (MT)-based transport a critical aspect of virus replication. Indeed, almost as soon as these filaments were identified and characterized, virus particles were observed proximal to "microtubuli," with evidence that MTassociated proteins (MAPs) might mediate this association. Chemicals that disrupt MT networks, still commonly used today, were reported to suppress virus infection. Moreover, either infection or expression of viral proteins was observed to alter the organization of these networks, suggesting that MTs not only facilitated infection but were also likely to be actively manipulated by viruses. In subsequent decades an enormous body of work helped unravel how virus particles exploit MT motors to traffic within infected cells, and we direct readers to a recent review of this subject (1). Here, we discuss recent advances in our understanding of how MTs themselves are regulated and function during infection, limiting this minireview to some illustrative examples in each case. TWO ENDS TO THE STORY: THE BASICS OF MT POLARITY AND ORGANIZATIONMTs form through the polymerization of ␣/␤-tubulin heterodimers into polarized filaments that have minus and plus ends (Fig. 1A and B). MTs nucleate through minus-end seeding at MT-organizing cen...

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The aphid transmission factor of cauliflower mosaic virus forms a stable complex with microtubules in both insect and plant cells

Cited by 41 publications

References 32 publications

Intracellular distribution of viral gene products regulates a complex mechanism of cauliflower mosaic virus acquisition by its aphid vector

Intracellular distribution of viral gene products regulates a complex mechanism of cauliflower mosaic virus acquisition by its aphid vector

The Cauliflower Mosaic Virus Protein P6 Forms Motile Inclusions That Traffic along Actin Microfilaments and Stabilize Microtubules

Microtubule Regulation and Function during Virus Infection

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